RING domain-deficient BRCA1 promotes PARP inhibitor and platinum resistance

Journal of Clinical Investigation

Volumn 126, Issue 8, 2016, Pages 3145-3157

  Wang, Yifan ^a   Krais, John J ^a   Bernhardy, Andrea J ^a   Nicolas, Emmanuelle ^a   Cai, Kathy Q ^a   Harrell, Maria I ^b   Kim, Hyoung H ^c   George, Erin ^c   Swisher, Elizabeth M ^b   Simpkins, Fiona ^c   Johnson, Neil ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; CISPLATIN; METHIONINE; MITOMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PACLITAXEL; PLATINUM; RING FINGER PROTEIN; RUCAPARIB; BRCA1 PROTEIN, HUMAN; MONOCLONAL ANTIBODY; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER CELL LINE; BREAST CARCINOMA; CANCER CHEMOTHERAPY; CANCER PATIENT; CANCER RECURRENCE; CANCER RESISTANCE; CELL CLONE; CHEMOSENSITIVITY; CODON; CONTROLLED STUDY; DRUG MECHANISM; FEMALE; FRAMESHIFT MUTATION; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; GERMLINE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; IRRADIATION; MOUSE; NONHUMAN; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVERTANT; RING FINGER MOTIF; SINGLE DRUG DOSE; SKIN METASTASIS; TRANSLATION REGULATION; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; BREAST NEOPLASMS; CANCER TRANSPLANTATION; CELL NUCLEUS; CHEMISTRY; CRISPR CAS SYSTEM; DRUG RESISTANCE; EXON; METABOLISM; MUTATION; NONOBESE DIABETIC MOUSE; PROTEIN DOMAIN; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CISPLATIN; CRISPR-CAS SYSTEMS; DRUG RESISTANCE, NEOPLASM; EXONS; FEMALE; GERM-LINE MUTATION; HUMANS; MICE; MICE, INBRED NOD; MUTATION; NEOPLASM TRANSPLANTATION; PLATINUM; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN DOMAINS;

EID: 84987837937     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI87033     Document Type: Article

References (58)

1. Szabo CI, King MC. Inherited breast and ovarian cancer. Hum Mol Genet. 1995;4(spec no):1811-1817.
2. Friedman LS, et al. Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families. Nat Genet. 1994;8(4):399-404.
3. Yang X, Lippman ME. BRCA1 and BRCA2 in breast cancer. Breast Cancer Res Treat. 1999;54(1):1-10.
4. Petrucelli N, Daly MB, Feldman GL. Hereditary breast and ovarian cancer due to mutations in BRCA1 and BRCA2. Genet Med. 2010;12(5):245-259.
5. Roy R, Chun J, Powell SN. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer. 2012;12(1):68-78.
6. Huen MS, Sy SM, Chen J. BRCA1 and its toolbox for the maintenance of genome integrity. Nat Rev Mol Cell Biol. 2010;11(2):138-148.
7. Jiang Q, Greenberg RA. Deciphering the BRCA1 Tumor Suppressor Network. J Biol Chem. 2015;290(29):17724-17732.
8. Moynahan ME, Chiu JW, Koller BH, Jasin M. Brca1 controls homology-directed DNA repair. Mol Cell. 1999;4(4):511-518.
9. Bryant HE, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434(7035):913-917.
10. Farmer H, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434(7035):917-921.
11. Moynahan ME, Cui TY, Jasin M. Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer Res. 2001;61(12):4842-4850.
12. Quinn JE, et al. BRCA1 functions as a differential modulator of chemotherapy-induced apoptosis. Cancer Res. 2003;63(19):6221-6228.
13. Silver DP, et al. Efficacy of neoadjuvant Cisplatin in triple-negative breast cancer. J Clin Oncol. 2010;28(7):1145-1153.
14. Safra T, Rogowski O, Muggia FM. The effect of germ-line BRCA mutations on response to chemotherapy and outcome of recurrent ovarian cancer. Int J Gynecol Cancer. 2014;24(3):488-495.
15. Jayson GC, Kohn EC, Kitchener HC, Ledermann JA. Ovarian cancer. Lancet. 2014;384(9951):1376-1388.
16. Scott CL, Swisher EM, Kaufmann SH. Poly (ADP-ribose) polymerase inhibitors: recent advances and future development. J Clin Oncol. 2015;33(12):1397-1406.
17. Kaufman B, et al. Olaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutation. J Clin Oncol. 2015;33(3):244-250.
18. Ledermann J, et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 2014;15(8):852-861.
19. Luvero D, Milani A, Ledermann JA. Treatment options in recurrent ovarian cancer: latest evidence and clinical potential. Ther Adv Med Oncol. 2014;6(5):229-239.
20. Ledermann JA, Kristeleit RS. Optimal treatment for relapsing ovarian cancer. Ann Oncol. 2010;21(suppl 7):vii218-vii222.
21. Lord CJ, Ashworth A. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat Med. 2013;19(11):1381-1388.
22. Norquist B, et al. Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol. 2011;29(22):3008-3015.
23. Sakai W, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008;451(7182):1116-1120.
24. Edwards SL, et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature. 2008;451(7182):1111-1115.
25. Patch AM, et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature. 2015;521(7553):489-494.
26. Rottenberg S, et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc Natl Acad Sci U S A. 2008;105(44):17079-17084.
27. Bunting SF, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 2010;141(2):243-254.
28. Bouwman P, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol. 2010;17(6):688-695.
29. Jaspers JE, et al. Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors. Cancer Discov. 2013;3(1):68-81.
30. Johnson N, et al. Stabilization of mutant BRCA1 protein confers PARP inhibitor and platinum resistance. Proc Natl Acad Sci U S A. 2013;110(42):17041-17046.
31. Drost R, et al. BRCA1 RING function is essential for tumor suppression but dispensable for therapy resistance. Cancer Cell. 2011;20(6):797-809.
32. Shakya R, et al. BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 2011;334(6055):525-528.
33. Friedman LS, et al. Novel inherited mutations and variable expressivity of BRCA1 alleles, including the founder mutation 185delAG in Ashkenazi Jewish families. Am J Hum Genet. 1995;57(6):1284-1297.
34. Struewing JP, et al. The carrier frequency of the BRCA1 185delAG mutation is approximately 1 percent in Ashkenazi Jewish individuals. Nat Genet. 1995;11(2):198-200.
35. Elstrodt F, et al. BRCA1 mutation analysis of 41 human breast cancer cell lines reveals three new deleterious mutants. Cancer Res. 2006;66(1):41-45.
36. Ignatoski KM, Ethier SP. Constitutive activation of pp125fak in newly isolated human breast cancer cell lines. Breast Cancer Res Treat. 1999;54(2):173-182.
37. Walsh T, et al. Mutations in 12 genes for inherited ovarian, fallopian tube, and peritoneal carcinoma identified by massively parallel sequencing. Proc Natl Acad Sci U S A. 2011;108(44):18032-18037.
38. Buisson M, Anczuków O, Zetoune AB, Ware MD, Mazoyer S. The 185delAG mutation (c.68-69delAG) in the BRCA1 gene triggers translation reinitiation at a downstream AUG codon. Hum Mutat. 2006;27(10):1024-1029.
39. Gebauer F, Hentze MW. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol. 2004;5(10):827-835.
40. Kozak M. Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol Cell Biol. 1989;9(11):5134-5142.
41. Kozak M. Constraints on reinitiation of translation in mammals. Nucleic Acids Res. 2001;29(24):5226-5232.
42. Hinnebusch AG. The scanning mechanism of eukaryotic translation initiation. Annu Rev Biochem. 2014;83:779-812.
43. Powley IR, et al. Translational reprogramming following UVB irradiation is mediated by DNAPKcs and allows selective recruitment to the polysomes of mRNAs encoding DNA repair enzymes. Genes Dev. 2009;23(10):1207-1220.
44. Joukov V, Chen J, Fox EA, Green JB, Livingston DM. Functional communication between endogenous BRCA1 and its partner, BARD1, during Xenopus laevis development. Proc Natl Acad Sci U S A. 2001;98(21):12078-12083.
45. Woolery KT, Mohamed M, Linger RJ, Dobrinski KP, Roman J, Kruk PA. BRCA1 185delAG mutation enhances interleukin-1β expression in ovarian surface epithelial cells. Biomed Res Int. 2015;2015:652017.
46. O'Donnell JD, Linger RJ, Kruk PA. BRCA1 185delAG mutant protein, BRAt, up-regulates maspin in ovarian epithelial cells. Gynecol Oncol. 2010;116(2):262-268.
47. Perrin-Vidoz L, Sinilnikova OM, Stoppa-Lyonnet D, Lenoir GM, Mazoyer S. The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Hum Mol Genet. 2002;11(23):2805-2814.
48. Ceccaldi R, et al. A unique subset of epithelial ovarian cancers with platinum sensitivity and PARP inhibitor resistance. Cancer Res. 2015;75(4):628-634.
49. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell. 2010;40(2):228-237.
50. Fabbro M, Rodriguez JA, Baer R, Henderson BR. BARD1 induces BRCA1 intranuclear foci formation by increasing RING-dependent BRCA1 nuclear import and inhibiting BRCA1 nuclear export. J Biol Chem. 2002;277(24):21315-21324.
51. Sobhian B, et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007;316(5828):1198-1202.
52. Wang B, et al. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 2007;316(5828):1194-1198.
53. Kim H, Chen J, Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007;316(5828):1202-1205.
54. Pathania S, et al. BRCA1 is required for postreplication repair after UV-induced DNA damage. Mol Cell. 2011;44(2):235-251.
55. Au WW, Henderson BR. The BRCA1 RING and BRCT domains cooperate in targeting BRCA1 to ionizing radiation-induced nuclear foci. J Biol Chem. 2005;280(8):6993-7001.
56. Chetrit A, Hirsh-Yechezkel G, Ben-David Y, Lubin F, Friedman E, Sadetzki S. Effect of BRCA1/2 mutations on long-term survival of patients with invasive ovarian cancer: the national Israeli study of ovarian cancer. J Clin Oncol. 2008;26(1):20-25.
57. Seeger C, Sohn JA. Targeting Hepatitis B virus with CRISPR/Cas9. Mol Ther Nucleic Acids. 2014;3:e216.
58. Swisher EM, Sakai W, Karlan BY, Wurz K, Urban N, Taniguchi T. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res. 2008;68(8):2581-2586.